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Annals of Surgical Oncology 10:59-64 (2003)
© 2003 Society of Surgical Oncology

ORIGINAL ARTICLES

Positron Emission Tomography Affects Surgical Management in Recurrent Colorectal Cancer Patients

Darius C. Desai, MD, Emanuel E. Zervos, MD, Mark W. Arnold, MD, William E. Burak, Jr., MD, Joseph Mantil, MD, PhD and Edward W. Martin, Jr., MD

From the Division of Surgical Oncology (DCD, MWA, WEB, EWM), Arthur G. James Cancer Hospital and Richard J. Solove Research Institute, The Ohio State University, Columbus, Ohio; Digestive Disorders Center (EEZ), University of South Florida, Tampa, Florida; and Department of Nuclear Medicine/PET (JM), Kettering Memorial Hospital, Dayton, Ohio.

Correspondence: Address correspondence and reprint requests to: Darius C. Desai, MD, St. Luke’s Hospital, 801 Ostrum St., Bethlehem, PA 18015; Fax: 610-954-6055; E-mail: desaid{at}slhn.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We determined the effect of positron emission tomography (PET) on surgical decision-making in patients with metastatic or recurrent colorectal cancer.

Methods: A total of 114 patients with advanced colorectal cancer were imaged with computed tomography (CT) and PET scans. The PET and CT scans were independently interpreted before surgery and recorded.

Results: Forty-two of the 114 patients had resectable disease on the basis of CT. PET altered therapy in 17 (40%) of these 42 patients on the basis of the following results: extrahepatic disease (n = 9), bilobar involvement (n = 3), thoracic involvement (n = 5), retroperitoneal lymphadenopathy (n = 2), bone involvement (n = 1), and supraclavicular disease (n = 1). In 25 patients with liver metastases only, PET found additional disease in 18 (72%), extrahepatic disease in 11, chest disease in 13, retroperitoneal lymphadenopathy in 4, and bone disease in 3. In five patients, both scans underestimated small-volume peritoneal metastases discovered at laparotomy.

Conclusions: PET altered therapy in 40% of patients. In patients with isolated liver involvement, 72% had more extensive disease that precluded surgical resection. PET scans should be used in the management of patients with recurrent colorectal cancer who are being considered for potentially curative surgery.

Key Words: PET • Colon cancer • Surgery • Recurrence


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Colorectal cancer is the second most prevalent cancer in the United States, accounting for approximately 150,000 new cases per year.1 Even after apparently curative resection, recurrences occur, usually within the first 2 to 3 years after surgery.2–5 More than 50,000 people will develop metastases from the primary tumor. At the time of recurrence, only 20% to 30% of patients are resectable for cure.6–9

Various modalities are used in the follow-up of patients with colorectal cancer. Carcinoembryonic antigen (CEA) is often used as a marker for recurrence. CEA is only 59% sensitive and 84% specific10 and does not provide any information as to the site or sites of recurrence. Computerized tomography (CT) scans are only 25% to 75% accurate in the follow-up of these patients.11 CT scans also underestimate the amount of tumor in isolated liver recurrences in 33% of patients, as well as the incidence of metastases to the peritoneum, mesentery, and lymph nodes.11–15

Previous studies have shown that >50% of patients with metastatic colorectal cancer brought to the operating room for attempted curative surgery were unable to undergo the planned operation because more extensive disease than anticipated was discovered at laparotomy.13,16–18 Accurate detection of an increased tumor burden by noninvasive means would allow curative surgery to be offered to a better-selected group of patients with metastatic colorectal cancer.

The malignant cells in colorectal cancer have an increase in glucose use.19–21 Positron emission tomography (PET) scans are now being used in the follow-up of patients with recurrent colorectal cancer.22 PET scans use [18F]2-fluoro-2-deoxy-D-glucose (FDG) by detecting increases in glucose metabolism. FDG is transported into cells by glucose transporter proteins. FDG-6-phosphate, its first metabolite after phosphorylation, cannot be converted into the fructose analog. This molecule has a negative charge and low membrane permeability and will accumulate intracellularly within the tumor cells.23

Whole-body PET scanning in the patient with recurrent colorectal cancer has been reported to be more sensitive and accurate than CT scans and CT portography. It is purported to be capable of differentiating among tumor, scar, fibrosis, and necrosis. Recent studies show PET scans to be >90% sensitive and accurate.22–28 Because of the increased availability of PET scans and their reported accuracy, as well as the inability of traditional modalities to determine the extent of recurrent colorectal cancer, this study was conducted to determine whether PET more accurately determined the extent of disease and affected surgical management.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From December 1998 to August 1999, 114 consecutive patients with colorectal cancer underwent CT scanning of the abdomen as well as a whole-body PET scan as part of their follow-up. This group included patients in routine follow-up as well as those undergoing work-up for a planned reoperation for metastasectomy. Patients with underlying inflammatory bowel disease and diabetes were excluded because of potential diagnostic overlap with PET. All CT and PET scans were performed within 2 months of each other. All patients were evaluated by a single surgeon.

All PET scans were acquired with a Siemens ECAT EXACTTM 922 (CTI, Inc., Knoxville, TN). All PET scans were performed by the same nuclear medicine technologist. Whole-body images were acquired 40 minutes after injection of 10 mCi of FDG injected in a fasting state. Patients were imaged from the neck to the rectum with an acquisition time of 10 minutes per bed by using a 40% transmission and 60% emission protocol. A separate acquisition was performed to evaluate the brain for metastatic disease. Fourier rebinding/ordered subsets reconstruction was performed on each whole-body scan. All PET scans were interpreted by two nuclear medicine radiologists with expertise in PET. Coronal, transaxial, and sagittal views were assessed to make a final interpretation. At the time of interpretation, the radiologists knew the previous CT scan results.

Most patients presented to our tertiary referral clinic with previous CT scans and reports. These films were not repeated unless the films were >2 months old, of poor quality, or performed without contrast. All CT scans, along with the PET imaging, were reviewed by our radiologists.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
One hundred fourteen patients with presumed recurrent colorectal cancer were imaged with conventional CT scans and PET scans. There were 60 men and 54 women, with a mean age of 61.8 years. Eighty-nine patients had presumed recurrent disease in the pelvis, and 25 had presumed isolated liver metastases.

Validation
To validate the use of PET in recurrent colorectal cancer, the first 26 patients undergoing PET scanning underwent laparotomy regardless of PET findings. In these initial 26 patients, CT predicted recurrent, resectable disease in 10 and was normal in 16 (increasing CEA with normal CT). Resectable disease was defined as local recurrence, fewer than four lesions per lobe of the liver, no extrahepatic disease in liver metastases, and the ability to get clear margins. PET scan confirmed resectable disease in the 10 patients in whom CT was positive and found disease in 13 additional patients, all confirmed at laparotomy. Three patients had normal PET and CT scans; each of them had diffuse peritoneal disease at the time of laparotomy (Table 1).


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  		TABLE 1. Operative validation of PET—initial 26 patients with presumed recurrent disease
 
PET/CT Negative Correlation
Forty-two of 114 patients had presumably resectable recurrences by CT scan. Of these 42 patients, PET found evidence of additional disease that would render them unresectable in 17 (40.4%). All 17 patients had presumed isolated liver recurrences by CT scan, and PET found extrahepatic disease in the abdomen or chest in 14, bilobar liver involvement in 3, and retroperitoneal disease in 2. None of these 17 patients underwent exploration as a result of PET findings (Fig. 1).



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  		FIG. 1. Clinical course of 114 patients with increasing carcinoembryonic antigen (CEA) undergoing computed tomography (CT) and positron emission tomography (PET) scans.

 
PET/CT Positive Correlation
PET and CT were in agreement in 25 patients. In these 25 patients, no evidence of disease could be found in 13 (occult increases in CEA; no surgery), 7 had isolated liver metastases, and 5 had isolated foci of recurrent disease in the abdomen.

Patients With Isolated Liver Disease by CT
Of the 25 patients with presumed isolated liver disease by CT scan, PET findings correlated with CT findings in 7. PET found additional disease in 17 patients, extrahepatic disease in 11, chest disease in 13, retroperitoneal lymphadenopathy in 4, and bone disease in 3. One patient with a positive CT scan had a negative PET scan (Table 2). Of the seven patients who were explored for liver resection, two underwent major lobar resection and five had resection aborted because of small-volume peritoneal disease (three with carcinomatosis and two with a positive portal lymph node).


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  		TABLE 2. CT/PET correlation in all patients and patients with isoloated hepatic metastases
 
Three-Year Follow-Up
The overall mean survival of the entire group of 114 patients was 16.1 months. For the 42 patients with what was thought to be resectable disease, it was 17.4 months. Of the 17 patients for whom CT predicted resectable disease and PET predicted unresectable disease, only 1 was alive at 3-year follow-up. This one patient had only multiple areas of retroperitoneal nodal disease. Of the patients who underwent curative surgery for isolated liver disease, all seven (two resected and five explored only) were dead at 3-year follow-up. Of the five patients with extrahepatic localized disease who underwent resection, all five were alive at 3-year follow-up.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Recurrent colorectal cancer carries a poor prognosis. The median survival is only 7 to 10 months without surgery.29,30 In patients who are surgical candidates, only 20% to 40% of patients are now resected for cure.6,7,31–33 One reason for this failure is the inability to detect all the disease at the time of reoperation. PET scans are now being used to follow up patients with recurrent colorectal cancer and other malignancies. This allows the extent of disease to be more accurately staged so more appropriate therapy can be initiated.

Small series have shown that PET scans change the management in 10% to 63% of patients, with most series reporting a change in 20% to 35%.24,28,34–37 In this study, 40% of patients were spared nontherapeutic laparotomy because of a positive PET scan. The decision to avoid surgery was based on previously published data, as well as on our own experience in 26 patients who underwent exploratory laparotomy to confirm PET scan findings (Table 1). In this validation portion of our series, chest disease on PET was confirmed with biopsy. Biopsy was positive in these 13 patients. After the validation portion of the study was complete, chest lesions were no longer biopsied unless they were the only site of activity on PET. The positive predictive value of 100% is the highest reported in the literature. Our specificity and negative predictive values were 0%, because there were no surgically confirmed true-negative scans in our experience. This is because the validation phase was performed on a small number of patients.

PET still has its limitations. PET scans are not able to detect small-volume disease and underestimate the extent of lesions <1 cm.24 In this series, five patients with colon cancer metastatic to the liver and a PET scan showing no evidence of extrahepatic disease were ultimately explored surgically. These five patients (20%) had peritoneal carcinomatosis or positive portal lymph nodes. Therefore, a negative PET scan with other positive imaging does not obviate the need for further surgery. The role of laparoscopy may seem to be intuitively beneficial here. In patients with potentially resectable disease by PET and CT scanning, our group uses laparoscopy to assess intra-abdominal burden before laparotomy. This may not always be possible, given existing adhesions and the extent of previous surgery. When laparoscopy is possible, it may help to avoid laparotomy and its inherent morbidities, even in patients with no evidence of disseminated disease by all available imaging modalities.

In contradistinction to the patient with a negative PET scan are those with a questionable finding by CT scanning and a positive PET scan. In this series, there were two patients with such CT findings on liver imaging and a positive PET scan in the liver without any extrahepatic disease. Surgical exploration of the abdomen along with intraoperative ultrasound examination of the liver did not reveal any metastatic or recurrent tumor. It may be that in time, detectable tumor will arise in the liver in the anatomical locations that were positive by PET scanning. Longer follow-up will be necessary to determine whether this is true. At 3-year follow-up, these two patients were alive and without evidence of disease. False-positive results may occur because FDG is not tumor specific. Leukocytes and macrophages will accumulate FDG.35 It is therefore important to view positive results in patients with known inflammatory bowel, diabetes, or lung disease, as well as patients who have undergone recent colonic polypectomy, with caution.34,38 These patients were excluded in this study.

In the 25 patients with presumed liver disease only, PET scanning revealed extrahepatic disease in 18 and did not add any new information about the tumor burden in the liver. The remaining seven patients were then explored. Only two of them underwent liver resection, because small-volume disease was found on abdominal exploration in the other five. This included both carcinomatosis and periportal lymph nodes containing tumor deposits. Our group performs extensive abdominal exploration before undertaking liver resection. Despite this, it is unclear why the resectability rate in these initial patients was only 8%. This is the lowest of any resectability rate that we know of reported in the literature. Neither of the resected patients survived 3 years. Neither had intra-arterial pumps placed. One had recurrences in the remaining lobe, and the other had liver failure while on an experimental protocol. This is in contrast to previously reported data showing a 77% 3-year survival for those patients undergoing hepatic resection after being staged by PET.37 It is impossible to draw a meaningful conclusion regarding survival on the basis of this study, with only two patients undergoing major lobar resection.

There were five patients with isolated, extrahepatic, localized recurrences. All five were explored operatively and were resected after no evidence of any other disease was found. All five had localized nodal recurrences. At 3-year follow-up, all five patients (100%) were alive and without disease.

There were eight people with a questionable CT scan finding in the abdomen, a normal CEA level, and a negative PET scan. The CT findings were sacral thickening, and it is impossible to distinguish recurrent tumor from scar or fibrosis. Because the PET scans were negative, these patients are being followed closely with serial imaging studies and tumor markers. To date, these eight patients are still alive without evidence of widespread recurrence.

In our series of 114 patients, therapeutic decision-making in 17 (40%) of 42 potentially operable patients was altered. In patients whose disease was confined to the liver according to conventional imaging studies, the PET scan results altered therapy in 78%. This is greater than has been previously reported.38 The information obtained with PET scans allowed surgery to be avoided in patients in whom it could not help. This provided not only an improvement in the quality of life of these patients, but also a potential cost savings. These data suggest that PET scans provide more accurate preoperative information than traditional CT scans. We conclude that PET scans should be used in the management of colorectal cancer patients as an integral part of the preoperative work-up when reoperative surgery is being considered. The information provided by PET scans complements available data from CT scans. Because of both PET and CT scannings’ inability to detect peritoneal carcinomatosis, laparoscopy should be the starting point of operative exploration. This allows laparotomy to be offered to better-selected patients with a higher chance of cure, while avoiding laparotomy in patients with diffuse disease and no chance for improvement in survival (Fig. 2).



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  		FIG. 2. Algorithm for recurrent colorectal cancer.

 


   Footnotes
 
This study evaluated the efficacy of positron emission tomography (PET) versus computed tomography scanning and its effect on surgical management in recurrent or metastatic colorectal cancer. PET scanning provided additional information to the surgeon, helping with decision-making in this difficult group of patients.

Received for publication May 2, 2002. Accepted for publication August 23, 2002.


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 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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